Athena Akrami

Converging Neuronal Activity in Inferior Temporal Cortex during the Classification of Morphed Stimuli

How does the brain dynamically convert incoming sensory data into a representation useful for classification? Neurons in inferior temporal (IT) cortex are selective for complex visual stimuli, but their response dynamics during perceptual classification is not well understood. We studied IT dynamics in monkeys performing a classification task. The monkeys were shown visual stimuli that were morphed (interpolated) between pairs of familiar images. Their ability to classify the morphed images depended systematically on the degree of morph. IT neurons were selected that responded more strongly to one of the 2 familiar images (the effective image). The responses tended to peak ∼120 ms following stimulus onset with an amplitude that depended almost linearly on the degree of morph. The responses then declined, but remained above baseline for several hundred ms. This sustained component remained linearly dependent on morph level for stimuli more similar to the ineffective image but progressively converged to a single response profile, independent of morph level, for stimuli more similar to the effective image. Thus, these neurons represented the dynamic conversion of graded sensory information into a task-relevant classification. Computational models suggest that these dynamics could be produced by attractor states and firing rate adaptation within the population of IT neurons.

Tactile perception and working memory in rats and humans

Significance Many higher cognitive functions involve working memory (WM), the storage and manipulation of information across limited time intervals. Comparing the WM capacity of different species is a key step toward understanding the underlying brain mechanisms. This study uncovers previously unknown sensory WM abilities in rats. They received two vibratory stimuli on their whiskers, separated by a variable delay, and had to compare vibration features. In analogous experiments, human subjects compared two stimuli applied to the fingertip. The acuity shown by rats in judging stimulus differences and their WM proficiency (across delays of 8 s, the longest tested) overlapped those of humans. Sensory WM now joins other cognitive functions within the rodent repertoire, setting the stage for exploration of its neuronal coding. Primates can store sensory stimulus parameters in working memory for subsequent manipulation, but until now, there has been no demonstration of this capacity in rodents. Here we report tactile working memory in rats. Each stimulus is a vibration, generated as a series of velocity values sampled from a normal distribution. To perform the task, the rat positions its whiskers to receive two such stimuli, “base” and “comparison,” separated by a variable delay. It then judges which stimulus had greater velocity SD. In analogous experiments, humans compare two vibratory stimuli on the fingertip. We demonstrate that the ability of rats to hold base stimulus information (for up to 8 s) and their acuity in assessing stimulus differences overlap the performance demonstrated by humans. This experiment highlights the ability of rats to perceive the statistical structure of vibrations and reveals their previously unknown capacity to store sensory information in working memory.

Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination.

Rhythms with time scales of multiple cycles per second permeate the mammalian brain, yet neuroscientists are not certain of their functional roles. One leading idea is that coherent oscillation between two brain regions facilitates the exchange of information between them. In rats, the hippocampus and the vibrissal sensorimotor system both are characterized by rhythmic oscillation in the theta range, 5–12 Hz. Previous work has been divided as to whether the two rhythms are independent or coherent. To resolve this question, we acquired three measures from rats—whisker motion, hippocampal local field potential (LFP), and barrel cortex unit firing—during a whisker-mediated texture discrimination task and during control conditions (not engaged in a whisker-mediated memory task). Compared to control conditions, the theta band of hippocampal LFP showed a marked increase in power as the rats approached and then palpated the texture. Phase synchronization between whisking and hippocampal LFP increased by almost 50% during approach and texture palpation. In addition, a greater proportion of barrel cortex neurons showed firing that was phase-locked to hippocampal theta while rats were engaged in the discrimination task. Consistent with a behavioral consequence of phase synchronization, the rats identified the texture more rapidly and with lower error likelihood on trials in which there was an increase in theta-whisking coherence at the moment of texture palpation. These results suggest that coherence between the whisking rhythm, barrel cortex firing, and hippocampal LFP is augmented selectively during epochs in which the rat collects sensory information and that such coherence enhances the efficiency of integration of stimulus information into memory and decision-making centers.

Lateral thinking, from the Hopfield model to cortical dynamics

Self-organizing attractor networks may comprise the building blocks for cortical dynamics, providing the basic operations of categorization, including analog-to-digital conversion, association and auto-association, which are then expressed as components of distinct cognitive functions depending on the contents of the neural codes in each region. To assess the viability of this scenario, we first review how a local cortical patch may be modeled as an attractor network, in which memory representations are not artificially stored as prescribed binary patterns of activity as in the Hopfield model, but self-organize as continuously graded patterns induced by afferent input. Recordings in macaques indicate that such cortical attractor networks may express retrieval dynamics over cognitively plausible rapid time scales, shorter than those dominated by neuronal fatigue. A cortical network encompassing many local attractor networks, and incorporating a realistic description of adaptation dynamics, may be captured by a Potts model. This network model has the capacity to engage long-range associations into sustained iterative attractor dynamics at a cortical scale, in what may be regarded as a mathematical model of spontaneous lateral thought. This article is part of a Special Issue entitled: Neural Coding.

Posterior parietal cortex represents sensory history and mediates its effects on behaviour

Many models of cognition and of neural computations posit the use and estimation of prior stimulus statistics: it has long been known that working memory and perception are strongly impacted by previous sensory experience, even when that sensory history is not relevant to the current task at hand. Nevertheless, the neural mechanisms and regions of the brain that are necessary for computing and using such prior experience are unknown. Here we report that the posterior parietal cortex (PPC) is a critical locus for the representation and use of prior stimulus information. We trained rats in an auditory parametric working memory task, and found that they displayed substantial and readily quantifiable behavioural effects of sensory-stimulus history, similar to those observed in humans and monkeys. Earlier proposals that the PPC supports working memory predict that optogenetic silencing of this region would impair behaviour in our working memory task. Contrary to this prediction, we found that silencing the PPC significantly improved performance. Quantitative analyses of behaviour revealed that this improvement was due to the selective reduction of the effects of prior sensory stimuli. Electrophysiological recordings showed that PPC neurons carried far more information about the sensory stimuli of previous trials than about the stimuli of the current trial. Furthermore, for a given rat, the more information about previous trial sensory history in the neural firing rates of the PPC, the greater the behavioural effect of sensory history, suggesting a tight link between behaviour and PPC representations of stimulus history. Our results indicate that the PPC is a central component in the processing of sensory-stimulus history, and could enable further neurobiological investigation of long-standing questions regarding how perception and working memory are affected by prior sensory information.

Transformation of Perception from Sensory to Motor Cortex

Summary To better understand how a stream of sensory data is transformed into a percept, we examined neuronal activity in vibrissal sensory cortex, vS1, together with vibrissal motor cortex, vM1 (a frontal cortex target of vS1), while rats compared the intensity of two vibrations separated by an interstimulus delay. Vibrations were “noisy,” constructed by stringing together over time a sequence of velocity values sampled from a normal distribution; each vibration’s mean speed was proportional to the width of the normal distribution. Durations of both stimulus 1 and stimulus 2 could vary from 100 to 600 ms. Psychometric curves reveal that rats overestimated the longer-duration stimulus—thus, perceived intensity of a vibration grew over the course of hundreds of milliseconds even while the sensory input remained, on average, stationary. Human subjects demonstrated the identical perceptual phenomenon, indicating that the underlying mechanisms of temporal integration generalize across species. The time dependence of the percept allowed us to ask to what extent neurons encoded the ongoing stimulus stream versus the animal’s percept. We demonstrate that vS1 firing correlated with the local features of the vibration, whereas vM1 firing correlated with the percept: the final vM1 population state varied, as did the rat’s behavior, according to both stimulus speed and stimulus duration. Moreover, vM1 populations appeared to participate in the trace of the percept of stimulus 1 as the rat awaited stimulus 2. In conclusion, the transformation of sensory data into the percept appears to involve the integration and storage of vS1 signals by vM1.

Collicular circuits for flexible sensorimotor routing

Historically, cognitive processing has been thought to rely on cortical areas such as prefrontal cortex (PFC), with the outputs of these areas modulating activity in lower, putatively simpler spatiomotor regions, such as the midbrain superior colliculus (SC). Using a rat task in which subjects switch rapidly between task contexts that demand changes in sensorimotor mappings, we report a surprising role for the SC in non-spatial cognitive processes. Before spatial response choices could be formed, neurons in SC encoded task context more strongly than neurons in PFC, and bilateral SC silencing impaired behavioral performance. Once spatial choices could begin to be formed, SC neurons encoded the choice faster than PFC, while bilateral SC silencing no longer impaired choices. A set of dynamical models of the SC replicates our findings. Our results challenge cortically-focused views of cognition, and suggest that ostensibly spatiomotor structures can play central roles in non-spatiomotor cognitive processes.

Posterior parietal cortex represents sensory stimulus history and is necessary for its effects on behavior

Many models of cognition and of neural computations posit the use and estimation of prior stimulus statistics1–4: it has long been known that working memory and perception are strongly impacted by previous sensory experience, even when that sensory history is irrelevant for the current task at hand. Nevertheless, the neural mechanisms and brain regions necessary for computing and using such priors are unknown. Here we report that the posterior parietal cortex (PPC) is a critical locus for the representation and use of prior stimulus information. We trained rats in an auditory Parametric Working Memory (PWM) task, and found that rats displayed substantial and readily quantifiable behavioral effects of sensory stimulus history, similar to those observed in humans5,6 and monkeys7. Earlier proposals that PPC supports working memory8,9 predict that optogenetic silencing of this region would impair behavior in our working memory task. Contrary to this prediction, silencing PPC significantly improved performance. Quantitative analyses of behavior revealed that this improvement was due to the selective reduction of the effects of prior sensory stimuli. Electrophysiological recordings showed that PPC neurons carried far more information about sensory stimuli of previous trials than about stimuli of the current trial. Furthermore, the more information about previous trial sensory history in the neural firing rates of a given rat’s PPC, the greater the behavioral effect of sensory history in that rat, suggesting a tight link between behavior and PPC representations of stimulus history. Our results indicate that the PPC is a central component in the processing of sensory stimulus history, and open a window for neurobiological investigation of long-standing questions regarding how perception and working memory are affected by prior sensory information.

Sensation of a “Noisy” Whisker Vibration in Rats

To provide a biological framework to be later applied in robotics, we have devised a delayed comparison task in which subjects discriminate between pairs of vibration delivered either to their whiskers, in rats, or fingertips, in human, with a delay inserted between the two stimuli. The task is to compare two successive stimuli, with different position standard deviations defined by σ1 and σ2. By varying the stimulus duration we have observed that rats’ performance improves for longer stimuli, suggesting that for stimuli with a probabilistic structure, evidence can be accumulated over time. On the other hand a change in stimulus duration biased human subjects. This experiment constrains models for the integration of tactile information in robotics.

Hippocampal population dynamics underlying memory trace activation in a tactile classification task

Hippocampal neuronal ensemble activity appears to play an important role in establishment of spatial and non-spatial episodic memories [1] and [2]. In particular, CA1 region of the hippocampus is well known to be a crucial site for processing associative memories which typically contain information about what, where, and when major behavioral events occurred [3]. In simple navigation tasks, it was shown that different spatial information can unfold in time either by complete reorganization of hippocampal place code in which both place and rate of firing take statistically independent values (global remapping, [4] and[5]) or instead, through minor modulation of firing rates in a same neural assembly (rate remapping, [4] and [5]). But to date, there is no evidence how CA1 ensembles remap to code different phases of a sensory, in particular tactile, memory task, at population level. Previously, it was shown how “single” cells in CA1 adapt an independent coding to represent tactile and reward location information [6]. This finding indicates that hippocampal neurons did not encode textured stimuli as physical objects along specific dimensions (e.g. coarseness), but as meaningful events in conjunction with the location in which they appeared. Moreover, the coding properties of neurons did not “follow” them across contexts. Here, we further analyzed population dynamics underlying this independence coding and explore both quantitative and qualitative differences between information content of single unit activities versus population vector. On each trial the rat touched a textured plate with its whiskers, and then turned towards the Left or Right water spout. Firstly, we measured the degree of rate-remapping, due to task-induced changes in population activity. The kolmogorov-smirnov distance between the empirical firing rate distribution of each single cell, collapsed in time and trial, and different null hypotheses, based on different assumptions on global remapping was computed. We also computed the correlation between pairs of population vectors taken from different times of each trial. These measures are independent of the relative magnitude of firing. Comparing the distributions of correlation values for entire set of population vectors between two trials, or two behaviorally different phases of each trial, provides an estimate of how much the ensemble code changes. When the rats experienced different phases of the task, however, the hippocampus encoded these changes robustly by changing the values of the components of the population vectors, without much, if any, change in the ensemble of recruited cells. Secondly, to see how presence of noise correlations may enhance coding property of the population, the performance of a non-linear classifier trained on few informative “single” cells was contrasted with a classifier trained on a) the complete set of cells and b) the principle components of the cell assembly. Thirdly, we applied trajectory-based activity classification of neural responses using Hidden Markov models, to segment the complete recording into a sequence of a few statistically discriminated hidden states, each correlated with different behavioral condition.